Ancient sharks may have pioneered the ability to taste bitterness in food

If a bite of dandelion greens or extra-dark chocolate makes you pucker, there’s good reason. Bitterness can indicate the presence of toxins in potential foods, and animals long ago honed the ability to ferret out harsh tastes.

But the ability to sense bitterness may be even older than many presumed, a new study finds. It likely first evolved in vertebrates roughly 460 million years ago, when sharks and other cartilaginous fishes separated from bony vertebrates like ourselves, researchers report today in the Proceedings of the National Academy of Sciences . The bitter taste receptor identified in a pair of shark species may mirror a sort of all-purpose bitterness detector that our common ancestor possessed.

“Given how quickly taste receptors change, to have this one receptor conserved over 460 million years, that’s pretty astounding,” says Craig Montell, a neurobiologist at the University of California, Santa Barbara who was not involved in the study. “The ability to react to the particular bitter chemicals that activate it must be really important.”

Humans and other bony vertebrates experience bitterness thanks to taste 2 receptors, or T2Rs, which are proteins that transmit taste information to the brain. But scientists had never found T2Rs in cartilaginous vertebrates such as sharks and rays. That led many to assume these receptors had evolved after their lineage split from the bony vertebrates. Yet sharks and other cartilaginous fish do have smell receptors closely related to bitter taste receptors. That made Sigrun Korsching, a neurobiologist at the University of Cologne, wonder: Could bitter taste perception be even older than most believed?

To find out, she and colleagues examined 17 genomes from various species of sharks, skates, and sawfish. Twelve of these had genes that coded for taste receptors similar to T2Rs, which they dubbed T2R1s. In the lab, the researchers implanted genes for these receptors from two of the species—bamboo sharks and catsharks—into human kidney cells, then exposed them to 94 bitter substances. These included resveratrol, found in foods such as grapes, peanuts, and cranberries, and amarogentin, a compound from the gentian plant considered one of the most astringent tastes in the world.

“There is a liqueur in southern Germany called gentian schnapps that contains an extract of that plant,” says Maik Behrens, a molecular biologist at the Technical University of Munich and co-author of the new study. “It’s awful bitter, I can tell you.”

Seven bitter substances activated the receptors from both sharks, whereas an additional four activated only those of the catshark. Several of those compounds also trigger receptors in bony fish such as zebrafish and the “living fossil” coelacanth, and all of them taste bitter to humans. Whether these animals all experience the same taste sensations, however, isn’t known, Korsching says. “We can at least ask humans, but it’s really hard to ask the fish.”

The findings suggest the ability to sense bitter tastes may have evolved before these groups diverged from a common ancestor some 460 million years ago, the authors say. Although bony vertebrates went on to evolve multiple kinds of bitter taste receptors, Korsching and colleagues detected genes for just one T2R1 in the sharks’ genomes. This T2R1, they argue, may resemble early, catch-all bitter detectors, not yet specialized to discriminate between different shades of bitterness. (Coffee snobs they were not.)

The sharks’ receptors also perked up when exposed to bitter substances that would be created inside their bodies, such as bile acids. The authors suggest this indicates that bitterness detectors may have originated with a broader role than just taste, also helping facilitate bodily functions that involved bitter substances.

Montell doesn’t find that explanation “very satisfying.” The first vertebrate bitterness receptors, he argues, likely detected either internal or external substances, then gradually evolved to do both. “It was probably one or the other—how could it just instantly be doing both?” he says. Testing a wider range of bitter chemicals from both inside and outside the body, he adds, might clarify which function came first.

Huabin Zhao, an ecologist at the Wuhan University, agrees with the paper’s conclusion that bitterness tasting probably arose before the split between bony and cartilaginous vertebrates. But the fact that receptors from two relatively closely related sharks reacted to many of the same bitter compounds isn’t surprising, Zhao notes. He wishes they’d run the experiment with bitter taste receptors from more species—such as sawfish—to see whether it produced the same results. If so, that would offer more certainty that the ancestral bitter receptor truly resembled the sharks’ T2R1s.

Korsching admits some uncertainty will always remain. “I wouldn’t bet my soul on this being the ancestral [receptor],” she says. “But what we did was as good as it can get. We cannot dig out the fossil of a 500-million-year-old shark and extract the DNA.”